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Morpho-molecular characterization of Gyrodactylus parasites of farmed tilapia and their spillover to native fishes in Mexico

  • 1.

    Froese, R. & Pauly, D. FishBase. Species 2000 www.catalogueoflife.org/annual-checklist/2019 (2019).

  • 2.

    Vanhove, M. P. M. et al. Hidden biodiversity in an ancient lake: Phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites. Sci. Rep. 5, 13669. https://doi.org/10.1038/srep13669 (2015).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 3.

    Canonico, G. C., Arthington, A., McCrary, J. K. & Thieme, M. L. The effects of introduced tilapias on native biodiversity. Aquat. Conserv. Mar. Freshw. Ecosyst. 15, 463–483. https://doi.org/10.1002/aqc.699 (2005).

    Article 

    Google Scholar 

  • 4.

    Cassemiro, F. A. S., Bailly, D., Júnio da Graça, W. & Agostinho, A. A. The invasive potential of tilapias (Osteichthyes: Cichlidae) in the Americas. Hydrobiologia 817, 133–154. https://doi.org/10.1007/s10750-017-3471-1 (2018).

    Article 

    Google Scholar 

  • 5.

    Le-Roux, L. & Avenant-Oldewage, A. Checklist of the fish parasitic genus Cichlidogyrus (Monogenea), including its cosmopolitan distribution and host species. Afr. J. Aquat. Sci. 35, 21–36. https://doi.org/10.2989/16085914.2010.466632 (2010).

    Article 

    Google Scholar 

  • 6.

    Zhang, S. et al. Monogenean fauna of alien tilapias (Cichlidae) in south China. Parasite 26, 4. https://doi.org/10.1051/parasite/2019003 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 7.

    García-Vásquez, A. et al. Gyrodactylids (Gyrodactylidae, Monogenea) infecting Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae): A pan-global survey. Acta Parasitol. 55, 215–229. https://doi.org/10.2478/s11686-010-0042-2 (2010).

    Article 

    Google Scholar 

  • 8.

    Salgado-Maldonado, G. & Rubio-Godoy, M. Helmintos parásitos de peces de agua dulce introducidos (eds. Mendoza, R. & Koleff, P.) 269–285 (Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, 2014).

  • 9.

    Jiménez-García, M. I., Vidal-Martínez, V. M. & López-Jiménez, S. Monogeneans in introduced and native cichlids in México: Evidence for transfer. J. Parasitol. 87, 907–909. https://doi.org/10.1645/0022-3395(2001)087[0907:MIIANC]2.0.CO;2 (2001).

    Article 
    PubMed 

    Google Scholar 

  • 10.

    Salgado-Maldonado, G., Aguilar-Aguilar, R., Cabañas-Carranza, G., Soto-Galera, E. & Mendoza-Palmero, C. Helminth parasites in freshwater fish from the Papaloapan river basin, Mexico. Parasitol. Res. 96, 69–89. https://doi.org/10.1007/s00436-005-1315-9 (2005).

    Article 
    PubMed 

    Google Scholar 

  • 11.

    Soler-Jiménez, L. C., Paredes-Trujillo, A. I. & Vidal-Martínez, V. M. Helminth parasites of finfish commercial aquaculture in Latin America. J. Helminthol. 91, 110–136. https://doi.org/10.1017/S0022149X16000833 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 12.

    Mendoza-Garfias, B., García-Prieto, L. & Pérez-Ponce de León, G. Checklist of the Monogenea (Platyhelminthes) parasitic in Mexican aquatic vertebrates. Zoosystema 39, 501–598. https://doi.org/10.5252/z2017n4a5 (2017).

    Article 

    Google Scholar 

  • 13.

    Ek-Huchim, J. P., Jiménez-García, I., Pérez-Vega, J. A. & Rodríguez-Canul, R. Non-lethal detection of DNA from Cichlidogyrus spp. (Monogenea, Ancyrocephalinae) in gill mucus of the tilapia Oreochromis niloticus. Dis. Aquat. Org. 98, 155–162. https://doi.org/10.3354/dao02435 (2012).

    CAS 
    Article 

    Google Scholar 

  • 14.

    Paredes-Trujillo, A., Velázquez-Abunader, I., Torres-Irineo, E., Romero, D. & Vidal-Martínez, V. M. Geographical distribution of protozoan and metazoan parasites of farmed Nile tilapia Oreochromis niloticus (L.) (Perciformes: Cichlidae) in Yucatán, México. Parasites Vectors 9, 2–16. https://doi.org/10.1186/s13071-016-1332-9 (2016).

    CAS 
    Article 

    Google Scholar 

  • 15.

    Grano-Maldonado, M. I., Rodríguez-Santiago, M. A., García-Vargas, F., Nieves-Soto, M. & Soares, F. An emerging infection caused by Gyrodactylus cichlidarum Paperna, 1968 (Monogenea: Gyrodactylidae) associated with massive mortality on farmed tilapia Oreochromis niloticus (L.) on the Mexican Pacific Coast. Lat. Am. J. Aquat. Res. 46, 961–968. https://doi.org/10.3856/vol46-issue5-fulltext-9 (2018).

    Article 

    Google Scholar 

  • 16.

    Morales-Serna, F. N., Medina-Guerrero, R. M., Pimentel-Acosta, C., Ramírez-Tirado, J. H. & Fajer-Ávila, E. J. Parasite infections in farmed Nile tilapia Oreochromis niloticus in Sinaloa, Mexico. Comp. Parasitol. 85, 212–216. https://doi.org/10.1654/1525-2647-85.2.212 (2018).

    Article 

    Google Scholar 

  • 17.

    Mendoza-Franco, E. F., Caspeta-Mandujano, J. M. & Tapia-Osorio, M. Ecto and endo-parasitic monogeneans (Platyhelminthes) on cultured freshwater exotic fish species in the state of Morelos, South-Central Mexico. ZooKeys 776, 1–8. https://doi.org/10.3897/zookeys.776.26149 (2018).

    Article 

    Google Scholar 

  • 18.

    Zahradníčková, P., Barson, M., Luus-Powell, W. L. & Přikrylová, I. Species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) from Cichlids from Zambezi and Pimpopo river basins in Zimbawe and South Africa: Evidence for unexplored species richness. Syst. Parasitol. 93, 679–700. https://doi.org/10.1007/s11230-016-9652-x (2016).

    Article 
    PubMed 

    Google Scholar 

  • 19.

    García-Vásquez, A., Razo-Mendivil, U. & Rubio-Godoy, M. Triple trouble? Invasive poeciliid fishes carry the introduced tilapia pathogen Gyrodactylus cichlidarum in the Mexican highlands. Vet. Parasitol. 235, 37–40. https://doi.org/10.1016/j.vetpar.2017.01.014 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 20.

    Harris, P. D., Shinn, A. P., Cable, J., Bakke, T. A. & Bron, J. GyroDb: Gyrodactylid monogeneans on the web. Trends Parasitol. 24, 109–111. https://doi.org/10.1016/j.pt.2007.12.004 (2008).

    Article 
    PubMed 

    Google Scholar 

  • 21.

    Shinn, A. P. et al. GyroDb World Wide Web electronic publication. http://www.gyrodb.net (2011).

  • 22.

    García-Vásquez, A., Hansen, H. & Shinn, A. P. A revised description of Gyrodactylus cichlidarum Paperna, 1968 (Gyrodactylidae) from the Nile tilapia, Oreochromis niloticus niloticus (Cichlidae), and its synonymy with G. niloticus Cone, Arthur et Bondad-Reantaso, 1995. Folia Parasitol. 54, 129–140. https://doi.org/10.14411/fp.2007.018 (2007).

    Article 

    Google Scholar 

  • 23.

    Paperna, I. Monogenetic trematodes collected from freshwater fish in Ghana. Second Rep. Bamidgeh 20, 88–90 (1968).

    Google Scholar 

  • 24.

    García-Vásquez, A., Hansen, H., Christison, K. W., Bron, J. E. & Shinn, A. P. Description of three new species of Gyrodactylus von Nordmann, 1832 (Monogenea) parasitising Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae). Acta Parasitol. 56, 20–33. https://doi.org/10.2478/s11686-011-0005-2 (2011).

    Article 

    Google Scholar 

  • 25.

    Přikrylová, I., Matějusová, I., Musilová, N. & Gelnar, M. Gyrodactylus species (Monogenea: Gyrodactylidae) on the cichlid fishes of Senegal, with the description of Gyrodactylus ergensi n. sp. from Mango tilapia, Sarotherodon galilaeus L. (Teleostei: Cichilidae). Parasitol. Res. 106, 1–6. https://doi.org/10.1007/s00436-009-1600-0 (2009).

    Article 
    PubMed 

    Google Scholar 

  • 26.

    Přikrylová, I., Vanhove, M. P. M., Janssens, S. B., Billeter, P. A. & Huyse, T. Tiny worms from a mighty continent: High diversity and new phylogenetic lineages of African monogeneans. Mol. Phylogenet. Evol. 67, 43–52. https://doi.org/10.1016/j.ympev.2012.12.017 (2012).

    Article 
    PubMed 

    Google Scholar 

  • 27.

    Šimková, A. Transmission of parasites from introduced tilapias: a new threat to endemic Malagasy ichthyofauna. Biol. Invasions 21, 803–819. https://doi.org/10.1007/s10530-018-1859-0 (2019).

    Article 

    Google Scholar 

  • 28.

    Ek-Huchim, J. P., Jiménez-García, I. & Rodríguez-Canul, R. DNA detection of Gyrodactylus spp. in skin mucus of Nile tilapia Orechromis niloticus. Vet. Parasitol. 272, 75–78. https://doi.org/10.1016/j.vetpar.2019.07.004 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 29.

    Rubio-Godoy, M., Paladini, G., Freeman, M. A., García-Vásquez, A. & Shinn, A. P. Morphological and molecular characterisation of Gyrodactylus salmonis (Platyhelminthes, Monogenea) isolates collected in Mexico from rainbow trout (Oncorhynchus mykiss Walbaum). Vet. Parasitol. 186, 289–300. https://doi.org/10.1016/j.vetpar.2011.11.005 (2012).

    Article 
    PubMed 

    Google Scholar 

  • 30.

    Garduño-Lugo, M., Granados-Alvarez, I., Olvera-Novoa, M. A. & Muñóz-Cordoba, G. Comparison of growth, fillet yield and proximate composition between Stirling Nile tilapia (wild type) (Oreochromis niloticus, Linnaeus) and red hybrid tilapia (Florida red tilapia x Stirling red O. niloticus) males. Aquac. Res. 34, 1023–1028. https://doi.org/10.1046/j.1365-2109.2003.00904.x (2003).

    Article 

    Google Scholar 

  • 31.

    Mendoza-Palmero, C., Blasco-Costa, I. & Pérez-Ponce de León, G. Morphological and molecular characterisation of a new species of Gyrodactylus von Nordmann, 1832 (Monogenoidea: Gyrodactylidae) of cichlid fishes (Perciformes) from Mexico. Parasitol. Int. 70, 102–111. https://doi.org/10.1016/j.parint.2019.02.009 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 32.

    Rubio-Godoy, M., Paladini, G., García-Vásquez, A. & Shinn, A. P. Gyrodactylus jarocho sp. nov. and Gyrodactylus xalapensis sp. nov. (Platyhelminthes: Monogenea) from Mexican poeciliids (Teleostei: Cyprinodontiformes), with comments on the known gyrodactylid fauna infecting poeciliid fish. Zootaxa 2509, 1–29. https://doi.org/10.11646/zootaxa.2509.1.1 (2010).

    Article 

    Google Scholar 

  • 33.

    García-Vásquez, A., Razo-Mendivil, U. & Rubio-Godoy, M. Morphological and molecular description of eight new species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) from poeciliid fishes, collected in their natural distribution range in the Gulf of Mexico slope, Mexico. Parasitol. Res. 114, 3337–3355. https://doi.org/10.1007/s00436-015-4559-z (2015).

    Article 
    PubMed 

    Google Scholar 

  • 34.

    Razo-Mendivil, U., García-Vásquez, A. & Rubio-Godoy, M. Spot the difference: Two cryptic species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) infecting Astyanax aeneus (Actinopterygii, Characidae) in Mexico. Parasitol. Int. 65, 389–400. https://doi.org/10.1016/j.parint.2016.05.009 (2016).

    Article 
    PubMed 

    Google Scholar 

  • 35.

    Rubio-Godoy, M. et al. To each his own: no evidence of gyrodactylid parasite host switches from invasive poeciliid fishes to Goodea atripinnis Jordan (Cyprinodontiformes: Goodeidae), the most dominant endemic freshwater goodeid fish in the Mexican Highlands. Parasites Vectors 9, 604. https://doi.org/10.1186/s13071-016-1861-2 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 36.

    García-Vásquez, A., Pinacho-Pinacho, C. D., Martínez-Ramírez, E. & Rubio-Godoy, M. Two new species of Gyrodactylus von Nordmann, 1832 from Profundulus oaxacae (Pisces: Profundulidae) from Oaxaca, Mexico, studied by morphology and molecular analyses. Parasitol. Int. 67, 517–527. https://doi.org/10.1016/j.parint.2018.03.003 (2018).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 37.

    García-Vásquez, A., Guzmán-Valdivieso, I., Razo-Mendivil, U. & Rubio-Godoy, M. Three new species of Gyrodactylus von Nordmann, 1832 described from Goodea atripinnis (Pisces: Goodeidae), an endemic freshwater fish from the central highlands of Mexico. Parasitol. Res. 117, 139–150. https://doi.org/10.1007/s00436-017-5680-y (2018).

    Article 
    PubMed 

    Google Scholar 

  • 38.

    García-Vásquez, A., Pinacho-Pinacho, C. P., Guzmán-Valdivieso, I., Salgado-Maldonado, G. & Rubio-Godoy, M. New species of Gyrodactylus von Nordmann, 1832 from native fish from Chiapas, Mexico, studied by morphology and molecular analyses. Acta Parasitol. 64, 551–565. https://doi.org/10.2478/s11686-019-00088-y (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 39.

    Pinacho-Pinacho, C. D. et al. Species delimitation of Gyrodactylus (Monogenea: Gyrodactylidae) infecting the southernmost cyprinids (Actinopterygii: Cyprinidae) in the New World. Parasitol. Res. 120, 831–848. https://doi.org/10.1007/s00436-020-06987-8 (2021).

    Article 
    PubMed 

    Google Scholar 

  • 40.

    Araujo, S. B. L. et al. Understanding host-switching by ecological fitting. PLoS ONE 10, e0139225. https://doi.org/10.1371/journal.pone.0139225 (2015).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 41.

    Friedman, M. et al. Molecular and fossil evidence place the origin of cichlid fishes long after Gondwanan rifting. Proc R Soc B. 280, 20131733. https://doi.org/10.1098/rspb.2013.1733 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 42.

    Zambrano, L., Martínez-Meyer, E., Menezes, N. & Peterson, A. T. Invasive potential of common carp (Cyprinus carpio) and Nile tilapia (Oreochromis niloticus) in American freshwater systems. Can. J. Fish. Aquat. Sci. 63, 1903–1910. https://doi.org/10.1139/F06-088 (2006).

    Article 

    Google Scholar 

  • 43.

    Bakke, T. A., Cable, J. & Harris, P. D. The biology of gyrodactylid monogeneans: The “Russian-Doll Killers”. Adv. Parasitol. 64, 161–460. https://doi.org/10.1016/s0065-308x(06)64003-7 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 44.

    Tripathi, A. The invasive potential of parasitic monogenoids (Platyhelminthes) via the aquarium fish trade: an appraisal with special reference to India. Rev. Aquacult. 6, 147–161. https://doi.org/10.1111/raq.12035 (2014).

    Article 

    Google Scholar 

  • 45.

    Huyse, T., Vanhove, M. P. M., Mombaerts, M., Volckaert, F. A. M. & Verreycken, H. Parasite introduction with an invasive goby in Belgium: Double trouble?. Parasitol. Res. 114, 2789–2793. https://doi.org/10.1007/s00436-015-4544-6 (2015).

    Article 
    PubMed 

    Google Scholar 

  • 46.

    Braga, M. P., Razzolini, E. & Boeger, W. A. Drivers of parasite sharing among Neotropical freshwater fishes. J. Anim. Ecol. 84, 487–497. https://doi.org/10.1111/1365-2656.12298 (2015).

    Article 
    PubMed 

    Google Scholar 

  • 47.

    Jovani, R. & Tella, J. L. Parasite prevalence and sample size: Misconceptions and solutions. Trends Parasitol. 22, 214–218. https://doi.org/10.1016/j.pt.2006.02.011 (2006).

    Article 
    PubMed 

    Google Scholar 

  • 48.

    Harris, P. D. & Cable, J. Gyrodactylus poeciliae n. sp. and G. milleri n. sp. (Monogenea: Gyrodactylidae) from Poecilia caucana (Steindachner) in Venezuela. Syst. Parasitol. 47, 79–85. https://doi.org/10.1023/A:1006413804061 (2000).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 49.

    Bowles, J. & McManus, D. P. Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RLFP method. Mol. Bioch. Parasitol. 57, 231–239. https://doi.org/10.1016/0166-6851(93)90199-8 (1993).

    CAS 
    Article 

    Google Scholar 

  • 50.

    Matejusová, I., Gelnar, M., McBeath, A. J. A., Collins, C. M. & Cunningham, C. O. Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). Int. J. Parasitol. 31, 738–745. https://doi.org/10.1016/S0020-7519(01)00176-X (2001).

    Article 
    PubMed 

    Google Scholar 

  • 51.

    Kearse, M. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 52.

    Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874. https://doi.org/10.1093/molbev/msw054 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 53.

    Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690. https://doi.org/10.1093/bioinformatics/btl446 (2006).

    CAS 
    Article 

    Google Scholar 

  • 54.

    Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542. https://doi.org/10.1093/sysbio/sys029 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 55.

    Rambaut, A. FigTree v1.3.1 Institute of Evolutionary Biology. University of Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/ (2006).

  • 56.

    Quantum GIS Development Team. Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project http://qgis.osgeo.org (2019).

  • 57.

    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing https://www.R-project.org/ (2017).


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